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The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness.

ABSTRACT: Insecticide-treated bed-nets (ITNs) control malaria by keeping mosquitoes from reaching people sleeping under a net and by killing mosquitoes. Most tests of ITNs consider their overall epidemiological outcome without considering the different behaviors underlying their effects. Here we consider one of these behaviors: that mosquitoes can bite through the net if its user is touching it. We assayed the ability of an insecticide-sensitive strain of the mosquito Anopheles gambiae to bite through a permethrin-treated or an untreated net, and their subsequent survival and fecundity. Despite the irritancy of permethrin, 71% of the mosquitoes took blood through the ITN (vs. 99% through the untreated net). The ITN reduced the time spent biting, the blood-meal size and the fecundity, and it killed about 15% of the mosquitoes within 24?hours of feeding (vs. 5% on the untreated net). However, the mosquito's survival was much higher than what we found in WHO cone assays, suggesting that the bloodmeal increased the mosquito's resistance to the insecticide. Thus, our results suggest that the irritancy and the toxicity of ITNs are reduced when mosquitoes contact and feed on their host, which will affect our understanding of the personal and community protection offered by the ITNs.

SUBMITTER: Hauser G

PROVIDER: S-EPMC6544760 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness.

Hauser Gaël G Thiévent Kevin K Koella Jacob C JC

Scientific reports 20190531 1

Insecticide-treated bed-nets (ITNs) control malaria by keeping mosquitoes from reaching people sleeping under a net and by killing mosquitoes. Most tests of ITNs consider their overall epidemiological outcome without considering the different behaviors underlying their effects. Here we consider one of these behaviors: that mosquitoes can bite through the net if its user is touching it. We assayed the ability of an insecticide-sensitive strain of the mosquito Anopheles gambiae to bite through a p ...[more]

PMID: 31148587

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Project description:Gene copy-number variations are widespread in natural populations, but investigating their phenotypic consequences requires contemporary duplications under selection. Such duplications have been found at the ace-1 locus (encoding the organophosphate and carbamate insecticides' target) in the mosquito Anopheles gambiae (the major malaria vector); recent studies have revealed their intriguing complexity, consistent with the involvement of various numbers and types (susceptible or resistant to insecticide) of copies. We used an integrative approach, from genome to phenotype level, to investigate the influence of duplication architecture and gene-dosage on mosquito fitness. We found that both heterogeneous (i.e., one susceptible and one resistant ace-1 copy) and homogeneous (i.e., identical resistant copies) duplications segregated in field populations. The number of copies in homogeneous duplications was variable and positively correlated with acetylcholinesterase activity and resistance level. Determining the genomic structure of the duplicated region revealed that, in both types of duplication, ace-1 and 11 other genes formed tandem 203kb amplicons. We developed a diagnostic test for duplications, which showed that ace-1 was amplified in all 173 resistant mosquitoes analyzed (field-collected in several African countries), in heterogeneous or homogeneous duplications. Each type was associated with different fitness trade-offs: heterogeneous duplications conferred an intermediate phenotype (lower resistance and fitness costs), whereas homogeneous duplications tended to increase both resistance and fitness cost, in a complex manner. The type of duplication selected seemed thus to depend on the intensity and distribution of selection pressures. This versatility of trade-offs available through gene duplication highlights the importance of large mutation events in adaptation to environmental variation. This impressive adaptability could have a major impact on vector control in Africa.

Project description:BackgroundInsecticide resistance poses a growing challenge to malaria vector control in Kenya and around the world. Following evidence of associations between the mosquito microbiota and insecticide resistance, the microbiota of Anopheles gambiae sensu stricto (s.s.) from Tulukuyi village, Bungoma, Kenya, with differing permethrin resistance profiles were comparatively characterized.MethodsUsing the CDC bottle bioassay, 133 2-3?day-old, virgin, non-blood fed female F1 progeny of field-caught An. gambiae s.s. were exposed to five times (107.5?µg/ml) the discriminating dose of permethrin. Post bioassay, 50 resistant and 50 susceptible mosquitoes were subsequently screened for kdr East and West mutations, and individually processed for microbial analysis using high throughput sequencing targeting the universal bacterial and archaeal 16S rRNA gene.Results47?% of the samples tested (n?=?133) were resistant, and of the 100 selected for further processing, 99?% were positive for kdr East and 1?% for kdr West. Overall, 84 bacterial taxa were detected across all mosquito samples, with 36 of these shared between resistant and susceptible mosquitoes. A total of 20 bacterial taxa were unique to the resistant mosquitoes and 28 were unique to the susceptible mosquitoes. There were significant differences in bacterial composition between resistant and susceptible individuals (PERMANOVA, pseudo-F?=?2.33, P?=?0.001), with presence of Sphingobacterium, Lysinibacillus and Streptococcus (all known pyrethroid-degrading taxa), and the radiotolerant Rubrobacter, being significantly associated with resistant mosquitoes. On the other hand, the presence of Myxococcus, was significantly associated with susceptible mosquitoes.ConclusionsThis is the first report of distinct microbiota in An. gambiae s.s. associated with intense pyrethroid resistance. The findings highlight differentially abundant bacterial taxa between resistant and susceptible mosquitoes, and further suggest a microbe-mediated mechanism of insecticide resistance in mosquitoes. These results also indicate fixation of the kdr East mutation in this mosquito population, precluding further analysis of its associations with the mosquito microbiota, but presenting the hypothesis that any microbe-mediated mechanism of insecticide resistance would be likely of a metabolic nature. Overall, this study lays initial groundwork for understanding microbe-mediated mechanisms of insecticide resistance in African mosquito vectors of malaria, and potentially identifying novel microbial markers of insecticide resistance that could supplement existing vector surveillance tools.

Dataset Information

The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness.

Publications

The ability of Anopheles gambiae mosquitoes to bite through a permethrin-treated net and the consequences for their fitness.

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